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Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis

Meiotic double-strand breaks (DSBs) are generated by the evolutionarily conserved SPO11 complex in the context of chromatin loops that are organized along axial elements (AEs) of chromosomes. However, how DSBs are formed with respect to chromosome axes and the SPO11 complex remains unclear in plants...

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Autores principales: Ku, Jia-Chi, Ronceret, Arnaud, Golubovskaya, Inna, Lee, Ding Hua, Wang, Chiting, Timofejeva, Ljudmilla, Kao, Yu-Hsin, Gomez Angoa, Ana Karen, Kremling, Karl, Williams-Carrier, Rosalind, Meeley, Robert, Barkan, Alice, Cande, W. Zacheus, Wang, Chung-Ju Rachel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7192515/
https://www.ncbi.nlm.nih.gov/pubmed/32310948
http://dx.doi.org/10.1371/journal.pgen.1007881
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author Ku, Jia-Chi
Ronceret, Arnaud
Golubovskaya, Inna
Lee, Ding Hua
Wang, Chiting
Timofejeva, Ljudmilla
Kao, Yu-Hsin
Gomez Angoa, Ana Karen
Kremling, Karl
Williams-Carrier, Rosalind
Meeley, Robert
Barkan, Alice
Cande, W. Zacheus
Wang, Chung-Ju Rachel
author_facet Ku, Jia-Chi
Ronceret, Arnaud
Golubovskaya, Inna
Lee, Ding Hua
Wang, Chiting
Timofejeva, Ljudmilla
Kao, Yu-Hsin
Gomez Angoa, Ana Karen
Kremling, Karl
Williams-Carrier, Rosalind
Meeley, Robert
Barkan, Alice
Cande, W. Zacheus
Wang, Chung-Ju Rachel
author_sort Ku, Jia-Chi
collection PubMed
description Meiotic double-strand breaks (DSBs) are generated by the evolutionarily conserved SPO11 complex in the context of chromatin loops that are organized along axial elements (AEs) of chromosomes. However, how DSBs are formed with respect to chromosome axes and the SPO11 complex remains unclear in plants. Here, we confirm that DSB and bivalent formation are defective in maize spo11-1 mutants. Super-resolution microscopy demonstrates dynamic localization of SPO11-1 during recombination initiation, with variable numbers of SPO11-1 foci being distributed in nuclei but similar numbers of SPO11-1 foci being found on AEs. Notably, cytological analysis of spo11-1 meiocytes revealed an aberrant AE structure. At leptotene, AEs of wild-type and spo11-1 meiocytes were similarly curly and discontinuous. However, during early zygotene, wild-type AEs become uniform and exhibit shortened axes, whereas the elongated and curly AEs persisted in spo11-1 mutants, suggesting that loss of SPO11-1 compromised AE structural maturation. Our results reveal an interesting relationship between SPO11-1 loading onto AEs and the conformational remodeling of AEs during recombination initiation.
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spelling pubmed-71925152020-05-11 Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis Ku, Jia-Chi Ronceret, Arnaud Golubovskaya, Inna Lee, Ding Hua Wang, Chiting Timofejeva, Ljudmilla Kao, Yu-Hsin Gomez Angoa, Ana Karen Kremling, Karl Williams-Carrier, Rosalind Meeley, Robert Barkan, Alice Cande, W. Zacheus Wang, Chung-Ju Rachel PLoS Genet Research Article Meiotic double-strand breaks (DSBs) are generated by the evolutionarily conserved SPO11 complex in the context of chromatin loops that are organized along axial elements (AEs) of chromosomes. However, how DSBs are formed with respect to chromosome axes and the SPO11 complex remains unclear in plants. Here, we confirm that DSB and bivalent formation are defective in maize spo11-1 mutants. Super-resolution microscopy demonstrates dynamic localization of SPO11-1 during recombination initiation, with variable numbers of SPO11-1 foci being distributed in nuclei but similar numbers of SPO11-1 foci being found on AEs. Notably, cytological analysis of spo11-1 meiocytes revealed an aberrant AE structure. At leptotene, AEs of wild-type and spo11-1 meiocytes were similarly curly and discontinuous. However, during early zygotene, wild-type AEs become uniform and exhibit shortened axes, whereas the elongated and curly AEs persisted in spo11-1 mutants, suggesting that loss of SPO11-1 compromised AE structural maturation. Our results reveal an interesting relationship between SPO11-1 loading onto AEs and the conformational remodeling of AEs during recombination initiation. Public Library of Science 2020-04-20 /pmc/articles/PMC7192515/ /pubmed/32310948 http://dx.doi.org/10.1371/journal.pgen.1007881 Text en © 2020 Ku et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Ku, Jia-Chi
Ronceret, Arnaud
Golubovskaya, Inna
Lee, Ding Hua
Wang, Chiting
Timofejeva, Ljudmilla
Kao, Yu-Hsin
Gomez Angoa, Ana Karen
Kremling, Karl
Williams-Carrier, Rosalind
Meeley, Robert
Barkan, Alice
Cande, W. Zacheus
Wang, Chung-Ju Rachel
Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis
title Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis
title_full Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis
title_fullStr Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis
title_full_unstemmed Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis
title_short Dynamic localization of SPO11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis
title_sort dynamic localization of spo11-1 and conformational changes of meiotic axial elements during recombination initiation of maize meiosis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7192515/
https://www.ncbi.nlm.nih.gov/pubmed/32310948
http://dx.doi.org/10.1371/journal.pgen.1007881
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